Role of the YehD fimbriae in the virulence-associated properties of enteroaggregative Escherichia coli
Main Author: | |
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Publication Date: | 2021 |
Other Authors: | , , , , , , , , , , , , , , , , , , |
Format: | Article |
Language: | eng |
Source: | Repositório Institucional da UNESP |
Download full: | http://dx.doi.org/10.1111/1462-2920.15737 http://hdl.handle.net/11449/229441 |
Summary: | The interaction of enteroaggregative Escherichia coli (EAEC) strains with the colonic gut mucosa is characterized by the ability of the bacteria to form robust biofilms, to bind mucin, and induce a local inflammatory response. These events are mediated by a repertoire of five different aggregative adherence fimbriae variants (AAF/I-V) typically encoded on virulence plasmids. In this study, we report the production in EAEC strains of a new YehD fimbriae (YDF), which is encoded by the chromosomal gene cluster yehABCD, also present in most E. coli strains. Immuno-labelling of EAEC strain 042 with anti-AAF/II and anti-YDF antibodies demonstrated the presence of both AAF/II and YDF on the bacterial surface. We investigated the role of YDF in cell adherence, biofilm formation, colonization of spinach leaves, and induction of pro-inflammatory cytokines release. To this aim, we constructed yehD deletion mutants in different EAEC backgrounds (strains 17-2, 042, 55989, C1010, 278-1, J7) each harbouring one of the five AAFs. The effect of the YDF mutation was strain dependent and AAF independent as the lack of YDF had a different impact on the phenotypes manifested by the different EAECs tested. Expression of the yehABCD operon in a E. coli K12 ORN172 showed that YDF is important for biofilm formation but not for adherence to HeLa cells. Lastly, screening of pro-inflammatory cytokines in supernatants of Caco-2 cells infected with EAEC strains 042 and J7 and their isogenic ΔyehD mutants showed that these mutants were significantly defective in release of IL-8 and TNF-α. This study contributes to the understanding of the complex and diverse mechanisms of adherence of EAEC strains and identifies a new potential target for preventive measures of gastrointestinal illness caused by EAEC and other E. coli pathogroups. |
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Role of the YehD fimbriae in the virulence-associated properties of enteroaggregative Escherichia coliThe interaction of enteroaggregative Escherichia coli (EAEC) strains with the colonic gut mucosa is characterized by the ability of the bacteria to form robust biofilms, to bind mucin, and induce a local inflammatory response. These events are mediated by a repertoire of five different aggregative adherence fimbriae variants (AAF/I-V) typically encoded on virulence plasmids. In this study, we report the production in EAEC strains of a new YehD fimbriae (YDF), which is encoded by the chromosomal gene cluster yehABCD, also present in most E. coli strains. Immuno-labelling of EAEC strain 042 with anti-AAF/II and anti-YDF antibodies demonstrated the presence of both AAF/II and YDF on the bacterial surface. We investigated the role of YDF in cell adherence, biofilm formation, colonization of spinach leaves, and induction of pro-inflammatory cytokines release. To this aim, we constructed yehD deletion mutants in different EAEC backgrounds (strains 17-2, 042, 55989, C1010, 278-1, J7) each harbouring one of the five AAFs. The effect of the YDF mutation was strain dependent and AAF independent as the lack of YDF had a different impact on the phenotypes manifested by the different EAECs tested. Expression of the yehABCD operon in a E. coli K12 ORN172 showed that YDF is important for biofilm formation but not for adherence to HeLa cells. Lastly, screening of pro-inflammatory cytokines in supernatants of Caco-2 cells infected with EAEC strains 042 and J7 and their isogenic ΔyehD mutants showed that these mutants were significantly defective in release of IL-8 and TNF-α. This study contributes to the understanding of the complex and diverse mechanisms of adherence of EAEC strains and identifies a new potential target for preventive measures of gastrointestinal illness caused by EAEC and other E. coli pathogroups.Department of Pediatrics University of Virginia School of MedicineUnidad de Investigación Médica en Enfermedades Infecciosas y Parasitarias Centro Médico Nacional Siglo XXI Instituto Mexicano de Seguro SocialCentro de Detección Biomolecular Benemérita Universidad Autónoma de PueblaUniversity of Florida Emerging Pathogens InstituteDepartamento de Patologia Universidade Federal do MaranhãoDepartamento de Microbiologia e Imunologia Instituto de Biociencias da UNESPFacultad de Estomatología Benemérita Universidad Autónoma de PueblaDepartamento de Biología Celular Centro de Investigaciones Avanzadas Instituto Politécnico NacionalCentro de Investigaciones en Ciencias Microbiológicas Benemérita Universidad Autónoma de PueblaLaboratory of Bacteriology Instituto ButantanDepartamento de Microbiologia e Imunologia Instituto de Biociencias da UNESPUniversity of Virginia School of MedicineInstituto Mexicano de Seguro SocialBenemérita Universidad Autónoma de PueblaEmerging Pathogens InstituteUniversidade Federal do MaranhãoUniversidade Estadual Paulista (UNESP)Instituto Politécnico NacionalInstituto ButantanSoria-Bustos, JorgeSaitz, WaleskaMedrano, AbrahamLara-Ochoa, CristinaBennis, ZinebMonteiro-Neto, Valeriodos Santos, Camilla ItaparyRodrigues, Josias [UNESP]Hernandes, Rodrigo T. [UNESP]Yáñez, Jorge A.Torres, JavierNavarro-García, FernandoMartínez-Laguna, YgnacioFontes Piazza, Roxane M.Munhoz, Danielle DiasCedillo, María L.Ares, Miguel A.De la Cruz, Miguel A.Nataro, James P.Girón, Jorge A.2022-04-29T08:32:35Z2022-04-29T08:32:35Z2021-01-01info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articlehttp://dx.doi.org/10.1111/1462-2920.15737Environmental Microbiology.1462-29201462-2912http://hdl.handle.net/11449/22944110.1111/1462-2920.157372-s2.0-85114024208Scopusreponame:Repositório Institucional da UNESPinstname:Universidade Estadual Paulista (UNESP)instacron:UNESPengEnvironmental Microbiologyinfo:eu-repo/semantics/openAccess2022-04-29T08:32:35Zoai:repositorio.unesp.br:11449/229441Repositório InstitucionalPUBhttp://repositorio.unesp.br/oai/requestopendoar:29462022-04-29T08:32:35Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)false |
dc.title.none.fl_str_mv |
Role of the YehD fimbriae in the virulence-associated properties of enteroaggregative Escherichia coli |
title |
Role of the YehD fimbriae in the virulence-associated properties of enteroaggregative Escherichia coli |
spellingShingle |
Role of the YehD fimbriae in the virulence-associated properties of enteroaggregative Escherichia coli Soria-Bustos, Jorge |
title_short |
Role of the YehD fimbriae in the virulence-associated properties of enteroaggregative Escherichia coli |
title_full |
Role of the YehD fimbriae in the virulence-associated properties of enteroaggregative Escherichia coli |
title_fullStr |
Role of the YehD fimbriae in the virulence-associated properties of enteroaggregative Escherichia coli |
title_full_unstemmed |
Role of the YehD fimbriae in the virulence-associated properties of enteroaggregative Escherichia coli |
title_sort |
Role of the YehD fimbriae in the virulence-associated properties of enteroaggregative Escherichia coli |
author |
Soria-Bustos, Jorge |
author_facet |
Soria-Bustos, Jorge Saitz, Waleska Medrano, Abraham Lara-Ochoa, Cristina Bennis, Zineb Monteiro-Neto, Valerio dos Santos, Camilla Itapary Rodrigues, Josias [UNESP] Hernandes, Rodrigo T. [UNESP] Yáñez, Jorge A. Torres, Javier Navarro-García, Fernando Martínez-Laguna, Ygnacio Fontes Piazza, Roxane M. Munhoz, Danielle Dias Cedillo, María L. Ares, Miguel A. De la Cruz, Miguel A. Nataro, James P. Girón, Jorge A. |
author_role |
author |
author2 |
Saitz, Waleska Medrano, Abraham Lara-Ochoa, Cristina Bennis, Zineb Monteiro-Neto, Valerio dos Santos, Camilla Itapary Rodrigues, Josias [UNESP] Hernandes, Rodrigo T. [UNESP] Yáñez, Jorge A. Torres, Javier Navarro-García, Fernando Martínez-Laguna, Ygnacio Fontes Piazza, Roxane M. Munhoz, Danielle Dias Cedillo, María L. Ares, Miguel A. De la Cruz, Miguel A. Nataro, James P. Girón, Jorge A. |
author2_role |
author author author author author author author author author author author author author author author author author author author |
dc.contributor.none.fl_str_mv |
University of Virginia School of Medicine Instituto Mexicano de Seguro Social Benemérita Universidad Autónoma de Puebla Emerging Pathogens Institute Universidade Federal do Maranhão Universidade Estadual Paulista (UNESP) Instituto Politécnico Nacional Instituto Butantan |
dc.contributor.author.fl_str_mv |
Soria-Bustos, Jorge Saitz, Waleska Medrano, Abraham Lara-Ochoa, Cristina Bennis, Zineb Monteiro-Neto, Valerio dos Santos, Camilla Itapary Rodrigues, Josias [UNESP] Hernandes, Rodrigo T. [UNESP] Yáñez, Jorge A. Torres, Javier Navarro-García, Fernando Martínez-Laguna, Ygnacio Fontes Piazza, Roxane M. Munhoz, Danielle Dias Cedillo, María L. Ares, Miguel A. De la Cruz, Miguel A. Nataro, James P. Girón, Jorge A. |
description |
The interaction of enteroaggregative Escherichia coli (EAEC) strains with the colonic gut mucosa is characterized by the ability of the bacteria to form robust biofilms, to bind mucin, and induce a local inflammatory response. These events are mediated by a repertoire of five different aggregative adherence fimbriae variants (AAF/I-V) typically encoded on virulence plasmids. In this study, we report the production in EAEC strains of a new YehD fimbriae (YDF), which is encoded by the chromosomal gene cluster yehABCD, also present in most E. coli strains. Immuno-labelling of EAEC strain 042 with anti-AAF/II and anti-YDF antibodies demonstrated the presence of both AAF/II and YDF on the bacterial surface. We investigated the role of YDF in cell adherence, biofilm formation, colonization of spinach leaves, and induction of pro-inflammatory cytokines release. To this aim, we constructed yehD deletion mutants in different EAEC backgrounds (strains 17-2, 042, 55989, C1010, 278-1, J7) each harbouring one of the five AAFs. The effect of the YDF mutation was strain dependent and AAF independent as the lack of YDF had a different impact on the phenotypes manifested by the different EAECs tested. Expression of the yehABCD operon in a E. coli K12 ORN172 showed that YDF is important for biofilm formation but not for adherence to HeLa cells. Lastly, screening of pro-inflammatory cytokines in supernatants of Caco-2 cells infected with EAEC strains 042 and J7 and their isogenic ΔyehD mutants showed that these mutants were significantly defective in release of IL-8 and TNF-α. This study contributes to the understanding of the complex and diverse mechanisms of adherence of EAEC strains and identifies a new potential target for preventive measures of gastrointestinal illness caused by EAEC and other E. coli pathogroups. |
publishDate |
2021 |
dc.date.none.fl_str_mv |
2021-01-01 2022-04-29T08:32:35Z 2022-04-29T08:32:35Z |
dc.type.status.fl_str_mv |
info:eu-repo/semantics/publishedVersion |
dc.type.driver.fl_str_mv |
info:eu-repo/semantics/article |
format |
article |
status_str |
publishedVersion |
dc.identifier.uri.fl_str_mv |
http://dx.doi.org/10.1111/1462-2920.15737 Environmental Microbiology. 1462-2920 1462-2912 http://hdl.handle.net/11449/229441 10.1111/1462-2920.15737 2-s2.0-85114024208 |
url |
http://dx.doi.org/10.1111/1462-2920.15737 http://hdl.handle.net/11449/229441 |
identifier_str_mv |
Environmental Microbiology. 1462-2920 1462-2912 10.1111/1462-2920.15737 2-s2.0-85114024208 |
dc.language.iso.fl_str_mv |
eng |
language |
eng |
dc.relation.none.fl_str_mv |
Environmental Microbiology |
dc.rights.driver.fl_str_mv |
info:eu-repo/semantics/openAccess |
eu_rights_str_mv |
openAccess |
dc.source.none.fl_str_mv |
Scopus reponame:Repositório Institucional da UNESP instname:Universidade Estadual Paulista (UNESP) instacron:UNESP |
instname_str |
Universidade Estadual Paulista (UNESP) |
instacron_str |
UNESP |
institution |
UNESP |
reponame_str |
Repositório Institucional da UNESP |
collection |
Repositório Institucional da UNESP |
repository.name.fl_str_mv |
Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP) |
repository.mail.fl_str_mv |
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1797790338551644160 |